The Incredible Lightness of Being Methane-Fuelled: Stable Isotopes Reveal Alternative Energy Pathways in Aquatic Ecosystems and Beyond

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The Incredible Lightness of Being Methane-Fuelled: Stable Isotopes Reveal Alternative Energy Pathways in Aquatic Ecosystems and Beyond View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector REVIEW published: 11 February 2016 doi: 10.3389/fevo.2016.00008 The Incredible Lightness of Being Methane-Fuelled: Stable Isotopes Reveal Alternative Energy Pathways in Aquatic Ecosystems and Beyond Jonathan Grey * Lancaster Environment Centre, Lancaster University, Lancaster, UK We have known about the processes of methanogenesis and methanotrophy for over 100 years, since the days of Winogradsky, yet their contributions to the carbon cycle were deemed to be of negligible importance for the majority of that period. It is only Edited by: in the last two decades that methane has been appreciated for its role in the global Jason Newton, carbon cycle, and stable isotopes have come to the forefront as tools for identifying Scottish Universities Environmental Research Centre, UK and tracking the fate of methane-derived carbon (MDC) within food webs, especially Reviewed by: within aquatic ecosystems. While it is not surprising that chemosynthetic processes David Bastviken, dominate and contribute almost 100% to the biomass of organisms residing within Linköping University, Sweden Blake Matthews, extreme habitats like deep ocean hydrothermal vents and seeps, way below the reach Eawag: Swiss Federal Institute of of photosynthetically active radiation, it is perhaps counterintuitive to find reliance upon Aquatic Science and Technology, MDC in shallow, well-lit, well-oxygenated streams. Yet, apparently, MDC contributes to Switzerland varying degrees across the spectrum from point sources to extremely diffuse sources. *Correspondence: Jonathan Grey Certainly a good proportion of the evidence for MDC contributing to freshwater food [email protected] webs comes from somewhere in the middle of that spectrum; from studies of seasonally stratifying lakes (mono- or dimictic) wherein, there is a defined gradient or boundary Specialty section: This article was submitted to at which anoxic meet oxic conditions and consequently allows for close coupling of Population Dynamics, methanogenesis and methanotrophy. However, even seemingly well-mixed (polymictic) a section of the journal Frontiers in Ecology and Evolution lakes have a contribution of MDC contributing to the benthic biomass, despite an almost continual supply of photosynthetic carbon being delivered from the surface. Aside Received: 31 October 2015 Accepted: 25 January 2016 from the fundamental importance of identifying the carbon sources fuelling biomass Published: 11 February 2016 production, stable isotopes have been integral in the tool box of palaeolimnologists Citation: seeking to identify how contributions from methane have waxed and waned over time. Grey J (2016) The Incredible Lightness of Being Methane-Fuelled: Stable Here, we synthesize the current state of knowledge in the use of stable isotopes to trace Isotopes Reveal Alternative Energy MDC in primarily freshwater ecosystems. Pathways in Aquatic Ecosystems and Beyond. Front. Ecol. Evol. 4:8. Keywords: methanotrophy, chironomids, zooplankton, carbon, food webs, greenhouse gas, biogeochemical doi: 10.3389/fevo.2016.00008 cycling, trophic transfer Frontiers in Ecology and Evolution | www.frontiersin.org 1 February 2016 | Volume 4 | Article 8 Grey Identifying and Tracking Methane in Food Webs A BRIEF SYNOPSIS ON THE GLOBAL routes by which CH4 produced in anoxic freshwater sediments IMPORTANCE OF METHANE IN AQUATIC may either by-pass or become incorporated into food webs is SYSTEMS, AND PARTICULARLY IN shown in Figure 1. FRESHWATERS COULD A METHANE PATHWAY BE The global carbon cycle was considered, until relatively recently, IMPORTANT TO SECONDARY to be solely the flux and storage of carbon between the PRODUCTION IN FOOD WEBS? atmosphere, and terrestrial and oceanic pools. Within the total carbon budget, it has been noted that despite their relatively Anoxic water and sediments are typically rich in organic small area, inland freshwaters make a considerable contribution matter compared to the overlying oxic water, and anoxic to the global methane (CH4) budget with emissions of CH4 from metabolism may account for a substantial part (20–60%) of the freshwaters being at least comparable to the terrestrial CH4 sink carbon metabolism and the heterotrophic microbial production (Battin et al., 2009). However, there is a considerable bias toward within freshwater environments (Hessen and Nygaard, 1992). data from lakes and other wetlands, and the role of rivers remains Methanogenesis in lakes has been reported corresponding to 30– poorly defined (Bastviken et al., 2011). Emissions of CH4 may be 80% of the anaerobic mineralization in waters and sediments small in terms of carbon, but one must consider that CH4 is a (Bastviken, 2009). While seasonal variability in CH4 oxidation is more potent greenhouse gas than CO2 over century time scales; known to be considerable, especially in dimictic lakes, between (Bastviken et al., 2011) estimated that global CH4 emissions 30–94% of the CH4 reaching oxygenated layers is reputedly expressed as CO2 equivalents correspond to at least 25% of the oxidized (Casper et al., 2000; Morana et al., 2015). In essence estimated terrestrial greenhouse gas sink. Our understanding of then, CH4 is a major product of the C mineralization in the global carbon cycle will only be complete if we include the lakes, and a large proportion may be converted to microbial flux of carbon through inland freshwaters (Cole et al., 2007; biomass equivalent in some instances to the total C fixation by Battin et al., 2009; Trimmer et al., 2012) getting to grips with heterotrophic bacteria and a significant proportion of primary methane-fuelling of food webs is an interesting and important production (Hessen and Nygaard, 1992; Bastviken et al., 2003). component of this. Indeed, (Cole, 2013) noted that “the role of Again, data from rivers are lacking, but across 15 rivers, in late methane in supporting food webs in lakes, and perhaps even summer, i.e., when one might expect the greatest contribution beyond their shores, has come as a surprise” and that “the from photosynthesis, (Shelley et al., 2014) conservatively notion that lake methane partially supports higher organisms in calculated that net methanotrophy was equivalent to between 1 surrounding terrestrial environments fundamentally changes our and 46% of benthic net photosynthetic production within the understanding of how aquatic food webs work.” gravel beds of chalkstreams. Couple this to the apparently high Methanogenesis is a universal terminal degradation process (50%) carbon conversion efficiency of methanotrophs (relative of organic matter in anoxic aquatic sediments when inorganic to 10–30%, typical for bacteria in detrital-based food webs), oxidants such as nitrate, ferric iron, or sulfate are depleted regardless of marked spatial and temporal changes in ambient (Conrad, 2005). Hence, in marine systems where there is methane concentration, and it suggests that methanotrophs can typically a high concentration of sulfate, the sulfur cycle sustain net production throughout the year (Trimmer et al., tends to dominate chemosynthesis, but in freshwaters where 2015). sulfate concentrations are typically lower (Hobbie, 1988) then The importance of a CH4 pathway to food webs might yet methanogenesis dominates. Stable isotopes have been an increase further under climate change. Increases in temperature incredibly useful tool in the identification and quantification forecast for the coming decades may have profound implications of methanogenic and methanotrophic pathways (Conrad, 2005) for the cycling of carbon in aquatic ecosystems due to the and further identifying the constituents of the complex microbial differential temperature dependencies of carbon fixation by community that is actively involved via stable isotope probing gross primary production (GPP) and carbon mineralization (SIP; e.g., He et al., 2012), but those aspects are not the focus of by ecosystem respiration (ER). For example, (Yvon-Durocher this review. Methane may be lost directly from the system via et al., 2010) showed that warming of 4◦C reduced the carbon ebullition or the recently hypothesized micro-bubble pathway, sequestration capacity of freshwater mesocosms by 13%, shifting stochastic processes notoriously difficult to quantify (Prairie and them toward net heterotrophy (i.e., net sources of CO2 to del Giorgio, 2013) or be effectively “piped” to the surface via the atmosphere) because ER responded more strongly to plants (Bergstrom et al., 2007; Sanders et al., 2007). Alternatively, temperature than GPP. They also found that methanogenesis or in addition, it may subsequently serve as an energy and C responded even more strongly than ER or GPP, with 20% more ◦ source for methanotrophs (methane oxidizing bacteria; MOB), of the GPP being accounted for by CH4 emissions with 4 C typically at oxic-anoxic boundaries (if anaerobic CH4 oxidation of warming (Yvon-Durocher et al., 2011). Benthic community is excluded) in the sediment, or in the water column (Kankaala structure and how that contributes to a host of ecosystem et al., 2007). It is essentially from this point in the cycle that processes, including microbial and macrofaunal decomposition stable isotopes have been key in tracing the use of methane- rates, was also clearly affected by such warming (Dossena et al., derived carbon (MDC) into, and through, food webs, particularly 2012). If it is assumed that delivery of organic matter does
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